E. G. BOBROV

Komarov Botanical Institute~ Academy of Sciences, Leningrad, U.S.S.R. (Privat address: 197022 Leningrad, P-22, Popova 2, W. 19, U.S.S.R.)

On Introgressive Hybridization and its Significance in the Evolution of Plants

K e y w o r d s

Introgresslve hybridizat ion, Evolution of plants, Picea, Larix, Pinus

A b s t r a c t

Hybr id forms arisen in the process of introgression are of low stabili ty. Changes in climate lead to absorption of hybr ids by the ancestor for which this change is most favourable. Though the forms created by hybr id introgression are able to exist for thousands or even millions of years, introgressive hybridizat ion in the cases known to us, as well as in the genera Picea, Larix, Pinus, has not opened and is not opening any evolut ionary prospects.

Ideas on introgressive hybridization have been forming during the last 40 years. However, they are still vague, because the range of phenomena concerning introgres- sive hybridization is not clearly defined, whereas the display of hybridization under natural conditions is extremely multiform. It explains contradictions in the assess- ment of introgressive hybridization in the evolutionary process. Thus, it is essential to retrace the development of ideas on this phenomenon, to determine more accurately its real nature, and to consider its significance in the evolutionary process.

This phenomenon was noticed almost simultaneously and quite independently by botanists in the U.S.S.R. and the U.S.A. It is appropriate, I think, to begin with native studies.

In 1934--1935 studying hornbeams (Carpinus) I observed many hybrids in a collection from Eastern Trans-Caucasia. Study showed that of six species of this region four were hybrids of two main species (BoBROV 1936). In 1943 in the vicinity of Kazan (Middle Volga) it was observed that representatives of the genera Picea,

Folia Geobot. Pbytotax., Praha, 17: 89--96, 198~

90 F O L I A G E O B O T A N I C A E T P H Y T O T A X O N O M I C A , 17, 1982

Pulsatilla, Primula, Rosa, widely distributed there, cannot be referred with certainty to this or that species. This could only be explained by hybridization of the species, encountered in a terr i tory which had formerly been free from glacier influence. Besides, it was supposed that this hybridization process had proceeded for millennia on vast and relatively free territories. That this phenomenon is not only local but could take place in other parts of the world, where the formation of the vegetat/on cover proceeded under similar conditions -- i.e. where contrary migrations of physio- logically compatible speciesmet, during hybrid introgression free habitats were present. The described phenomenon was then called hybrid nfixing of species (BoBROV 1944). My publication did not attract the at tention of Soviet botanists, but according to KATHERINE ESAU'S paper (1945) it was noticed by American dendrologists (WRmHT 1955) who paid special attention to spruce hybridization.

In 1958 G. E. GROSS~.T published a study on distribution of Cornus sanguinea in the the South-European part of the U.S.S.[{. and introgression of this Western species with the Eastern C. australis in the post-glacial period. He observed the absorption of the population of one Comus species by another. GRosseT pointed out tha t BOBROV'S hybrid mixing of species and ANDERSON'S introgressive hybridization reflect the same natural phenomenon. The American botanist and geneticist EDGAR A~DERSON (1949) began in 1938 to publish articles on the genetic analysis of the hybrid populations of Tradescantia, Phlox and Iris. His work on the introgressive hybridization of Juniperus was most important. ANDI~RSON spoke of this phenomenon in the same terms as we use for hybrid mixing of species; he connected it with species distribution caused by the Quaternary period and on a vast territory. There is no doubt that ANDERSON and BOBROV independently discovered and described the same phenomenon.

In 1959--1960 we drew attention to the Middle Siberian flora, supposing that the phenomenon of introgrcssive hybridization was well expressed there. Indeed, on territories adjoining the Baikal Lake (BoBRov 1961) we found on the base of herbarium data introgression in some pairs of Betula, Adenophora, Oxytropis species, in widely distributed species of Larix, Polygonum (Aconogon), Sanguisorba, and also in separate pairs of species from the genera Spiraea, Potentilla, Ribes, Vicia. This work has shown that under certain conditions introgressive hybridization has covered not only separate pairs of species but dozens of them, and that these species are the elements of vicarious formations; therefore we can speak of the "introgression" of the latter. When studying hybrids of Siberian and Dahurian larches a very import- ant phenomenon was observed -- absorption of the hybrid populations in due course, by those of the parental-ancestors for which the new conditions were more favourable. One more important conclusion was drawn -- for real evolution introgressive hybrid- ization has very restricted meaning.

In ANDERSON'S well-known review (ANDERSON 1949) the introgression of some species is discussed and methodological directions for field study are given. The author of the book positively avoids discussion of the importance of introgressive hybridization for evolution. In this first passage he writes: " I t passes no judgments on the importance of hybridization in evolution. . ." In the epilogue we read: "How important is introgressive hybridization? I do not know. One point seems fairly certain: its importance is paradoxical. The more imperceptible introgression becomes, the greater is its biological significance. I t may be of the greatest fundamental

B O B R O V : I N T R O G I ~ E S S I V E H Y B R I D I Z A T I O N 91

importance when by our present crude methods we can do no more than to demonstrate its existence."

In another work (A~Dm~so~ 1953) nothing is said on the importance of intro- gressive hybridization for evolution. Here the essence of the phenomenon itself is emphasized -- " the gradual infiltration of the germplasm of one species into that of another as a consequence of hybridization and repeated backcrossing". To this phenomenon the author relates the cases of common species hybridization, connected with the destruction of natural plant cover and even the origin of weeds and cultivated plants. I t is absolutely impossible to agree with many aspects. Proceeding from the formal definition of the phenomenon it may be possible to explain the hybrid origin of some cultivated plants and to relate here even the two-seasonal field experiments Of selectionists. However, it is fundamentally important to distinguish artificial selection from the natural one.

The definition of the phenomenon given by A~DERSON is purely genetical, our definition (BOBROV 1944) points out its botanical-geographicM aspect: introgressive hybridization (i.e. hybrid mixing of species) proceeds in natural conditions on vast territories during millennia in contrary migrations of physiologically compatible species and with ecological niches available.

The article by ANDERSON et ST~.BBI~S (1954) seemed to answer the question. However, it is declared in the article that the authors are far from conclusions on the general theory of evolution (p. 386) and that hybridization can produce three possible results: introgression, segregation of the new types without backcrosses and allo- polyploidy.

In his more detailed work STEBBI~S (1959), discussing the importance of hybridiza- tion in evolution, drew the conclusion that in hybridization only exceptionally -- by mutation or by isolation -- new types capable to give evolutional lines can be created. We would of course agree with this conclusion.

The prominent Soviet botanist M. G. PoPov was very much interested in problem of the importance of hybridization for evolution. In one of his earlier works (PoPov 1927) concerning the systematics of Eremostachya, Zygophyllum, Agropyrum and Elymus species he affirmed (p. 272) that "the formcreative process simultaneously captures a mass of individuals and develops on a vast terri tory. Distribution boundaries of some species are defined by coming into contact with other species which have hybrid effect on the former. Races and species can arise convergently by means of hybridization between similar pairs of species". Considering further the variability of Eremostachys eriocalyx, PoPov observed that crossing "can lead to the absorption by the new-comer of a species which was here before". This indicates tha t PoPov was the first investigator of our time who drew attention to introgressive hybridization in natural conditions.

The study of Pinaceae systematics has greatly contributed to the under standing of introgressive hybridization and to the elucidation of its evolutionary significance. In the genus Picea (BoBROV 1971, 1972a) 6 or 7 pairs of species in five regions of the northern hemisphere come into introgression; there on the vast territories not real species but their hybrid forms composed during the process of introgression appeared in the role of the former forest. In the North of Eastern Europe the west European P. abies and Siberian P. obovata are in introgression; in South China -- P. asperata and P. likiangensis; in the Soviet Far East -- P. obovata and P. a]anenM8, and also

92 FOLIA GEOBOTANICA ET PHYTOTAXOI~OMICA, 17,1982

the last and P. kora]ensis; in Western North America -- P. glauca and P. engelmanii; in Northern-Eastern America -- P. glauca and P. rubens.

The s tudy of the genus Picea has given an opportunity to know much new data. We observed that not closely related species but species referred to different species series or to different sections and even to different genera into introgression. I t was observed that in North Eastern Europe introgression is connected with the events of the Quaternary and Holocene periods. Warming in the second half of the Holocene led to the substitution and absorption of one spruce species - - as an edificator of one formation. In the indicated region spruce forest of the Siberian type (edificator P. obovata) is displaced by spruce forest of the West European type (edificator P. abies). I t has to be supposed that this process will proceed as long as climatic conditions are favourable. If they change and become more favourable for P. obovata, the process will be reversed.

One more important conclusion is drawn: five species of spruce of the section Omorilca are the products of intergenerie introgressive hybridization of boreal spruces (sect. Picea) and species of the genus Tsuga (sect. Hesperopeuce). Their introgressive hybridization could have taken place in Neogene when Tsugas were distributed over the whole of temperate Euroasias. This supposition on the hybridiza- tion of Picea and Tsuga in the Tert iary period is well-grounded for we know modern hybrids Tsuga-Picea in the Rocky Mountains of America and hybrids Tsuffa- Keteleeria in Southern China also. Distributions of all spruce species of the section Omorilca are insignificant -- they stretch for tens, seldom for 1--4 hundreds km (BoBaov 1971, Fig. 4; 1972a, Fig. 2), whereas in species of the type section they stretch across the continents for thousands of kilometres. I t is noteworthy that areas of some spruces, composed in hybrid introgression, stretch for hundreds and even thousands of kilometres. We may draw one more important conclusion: though the hybrids composed in its introgressive process do not create new evolutionary lines they are able to exist for millennia and even millions of years. We also consider that "Omorika" spruces can be synthesized by the hybridization of Picea species (section Picea) with Tsuga species (section Hesperopeuce).

A systematic study of the genus Larix (BoBROV 1972b) showed that in this genus introgressive hybridization is also a norm. In Eurasia there are five consider- able territories where larch forests are formed by hybrid swarms. Of 17 species belonging to the genus, 5--6 pairs of species are introgressively mixed. Their intro- gression can be referred to the Pleistocene and Holocene and even to the end of the Tert iary period. The product of hybrid introgression -- L. X polonica (L. deci- duaXL, sibirica) has a Carpathian-Transilvanian distribution area; L. Xczekanovskii (L. sibirica X L. gmelinii) is restricted to the region east of Yenisei from Taimyr up to Trans-Baikah the greater par t of the Far East is settled by L. X maritima (L. gmelinii X L. kamtschatica); L. ca]anderi X L. X maritima is confined to the North; L. X lubarskii (L. maritima X L. olgae) is in the South of the Primorje. The formation of L. X IJolonica is connected with the Pleistocene and its modern distri- bution area is residual populations absorbed by West European L. decidua. L. )< czekanovs~ii was composed in the Holocene and its modern area is the result of migration to the East in the second half of the Holocene. L. X maritima reflects the Holocene migration of L. gmelinii to the East and gradual absorption of L. kamtscha- tica; L. X maritima in its turn produces hybrid mixing in the North with L. ca]an-

B O B R O V : I N T R O G R E S S I V E H Y B R I D I Z A T I O N 93

deri, and in the South with L. olgae. Thus we observe that introgressive hybridi- zation in Larix and Picea has much in common. The following fact is striking: five Southern species of the genus Larix compose the section Multiseriales. Thier origin is hybridogenous -- they are the products of introgressive hybridization of boreal species of the genus Larix with some species of Pseudotsuga -- the cone structure proves it. There is also an intergenetie hybrid -- Larix--Pseudotsuga. The formation of larches of section Multiseriales must be attributed, as in spruces of Omorika section, to the end of Neogene. At present both of them are becoming extinct. I t is very interesting to note that the distribution of the two coincides (BOBROV 1972b, Fig. 4). I t indicates that creation of both of them is connected with the same physical and geographical events. Undoubtedly analogous formation took place within other genera inhabiting the same regions -- Himalayas, Southern China, Rocky Mountains. The investigators did not notice this phenomenon.

The experiment on synthesis of larches of the Multiseriales type carried out in our country is of great importance, though it should be cpnsidered as a preliminary one. On my advice L. A. KN~ZEVA (1978) crossed Larix sibirica X Pseudotsuqa taxi]olia. The obtained seeds obtuned were sown in 1972 and 1974 and the seedlings were grown on the plantation near Moscow in 1976. The height of the four-years hybrids was 15 to 85 cm. The larches of Multiseriales type are to grow from these hybrids. Thus we see that the study of introgressive hybridization in the Larix genus confirmed all the facts which had been found out during work on Picea genus, and some new facts were even added. Studying further Pinus systematics something new has emerged.

Some information on pine hybridization in China was given by Mmov (1967). He pointed out that Pinus tabulae/ormis (widely distributed in China) hybridizes with different species in various parts of periphery the area. Mmov writes (p. 553 to 554): "P. tabulae]ormis merges into P. yunnanensis; P. yunnanensis gradually merges into P. ]chasya, and in Assam, Upper Burma and adjoining Thailand all these pines are represented by one species". In this case introgression of species is to be supposed. For us P. tabulae/ormis var. pseudosylvestris is of a special interest; it is, as we understand it, the hybrid of this Chinese species with the European-Sibe- rian P. sylvestris. I t is distributed in the desert mountains of Outer Mongolia from where it may reach Khallingol (BoBROV 1978). In the southern par t of Primorje hybrid introgression between Korean-Japanese P. densiflora and European-Sibirian P. sylvestris, which recently reached the Eastern region of Khanka, was be observed (BoBROV 1975a). The pine composed there is called P. X/unebris and its populations inhabit Southern part of Primorje and the adjoining territories reaching 400--500 km in length.

Till recently the Caucasian pine of P. sylvestris type was a mystery. Our study has shown that a degree of isolation of P. sylvestris from the South European P. syl- vestris is connected with the development at the very end of Neogene of the Euxine botanical-geographical province. We suppose that the Euxine pine (P. kocMana) was introgressed twice. In Pleistocene the natural landscape, of which one of the elements was the pine forest of Russian Plain, reached the Caucasus, where as the boreal P. sylvestris distributed southward, forcing the Euxine pine out in the process of introgression. Warming at the end of Holocene turned that process back and forced out the boreal P. sylvestris from the Euxine province (BoBROV 1975b).

94 F O L I A G E O B O T A N I C A E T P H Y T O T A X O N O ~ I C A , 17, 198 2

The genus Pinus is divided into two subgenera -- Haploxylon and Diploxylon it is better to call them Strobus ad Pinus, respectively. Cedar pines are referred to the former, all others to the latter. However, there is a small group of pines series. Flexiles. containing two species, the Chinese P. armandii and American P. flexilis, which cannot be referred to either of the two subgenera. We may suppose that they originated as a result of species introgression which involved different genera (now subgenera). The introgression proceeded independently at the very end of Neogene in Eastern Asia and in the Rocky Mountains of Northern America. Series Flexiles is a link which connects both subgenera. If this link were absent there would to no doubts that cedars and other pines are different genera; we may suppose that they are connected by hybrid introgression.

All the above data enable us to make the following conclusion on introgressive hybridization and on its significance in evolution.

Introgressivc hybridization is a phenomenon connected with paleogeographical events; it proceeds on vast territories for millennia during the contrary migration of physiologically compatible species. The genetic base of the phenomenon is the penetration of the embryonic plasm of one species into that of another as a result of hybridization and backerosses. :Not the most closely related species but on the contrary those belonging to different series, to different sections and even to different genera come into introgression. :Not separate pairs of species but many species are involved in the introgressive hybridization in certain areas. The hybrid forms, composed during introgression, are sometimes distributed for hundreds and thousands of kilometres being formation dominants; they are able to exist for thousands and even millions of years. The contrary change of climatic conditions leads to the ab- sorption of hybrids, composed in the process of introgression, by the ancestor for which the change is more favourable. Thus the process of introgression can proceed back. The absorption of hybrid populations by the species-edificator reflects the displacement of one vicarious formation by another. Spruce forests af the Siberian type (edificator -- Picea abovata) in Eastern Europe are forced out by spruce forests of the West European type (edificator -- P. abies). The larch forests of Larix kamt- schaticainthe Far East aer forced out by the East Siberian larch forests of L. 9melinii. Introgressive hybridization which proceeded at the end of the Tert iary between Picea and Tsuga species, and also between Larix and Pseudotsuga species, led to the creation of the section Omorika spruces and the section Multiseriales larches. How- ever, it did not create evolutionary lines -- the Picea and Larix species of these sections obviously became extinct. The experiments to cross Larix sibirica and Pseudotsuga taxi/olia carried out in 1972 and 1974 proved the possibility of hybrid genesis of larches of the Multiseriales section. The introgressive hybridization irr each known case, as with forest forming Conifers -- Picea, Larix, Pinus, did not create stable forms and did not open up evolutionary perspectives.

SUMMARY

Introgressive hybridization is a phenomenon connected with paleogeographica]L events; it proceeds for millennia during the contrary migration of physiologically compatible species. The genetic base of the phenomenon is the penetration of th~

BOBROV:INTROGRESSIVE HYBRIDIZATION 95

embryon ic p lasm of one species into t h a t of ano ther as a resu l t Of hybr id i za t ion and back-crosses. N o t the most closely r e l a t ed species bu t on the c o n t r a r y species r e l a t ed to different species series of genera , to different sections and even to different genera come in to introgression. No t separa te pa i rs of species bu t m a n y species a re involved in in t rogress ive hyb r id i z a t i on in definite areas. The h y b r i d forms composed dur ing in t rogress ion a re somet imes d i s t r i bu t ed over h u n d r e d s and thousands of k i lometres , being fo rma t ion dominants ; t h e y are able to exis t for thousands a n d even mill ions of years . The con t r a ry change of c l imat ic condi- t ions leads to the abso rp t ion of hybr ids , composed in the process of in t rogress ion, b y the ances tor for which t ha t change is more favourable . Thus the process of in t rogress ion can p roceed back. The abso rp t ion of a h y b r i d popu la t ion b y the species edif icator ref lects the d i sp lacement of one vicar ious fo rma t ion b y another . Spruce forests of the S iber ian t ype (edif icator - - Pfcea obovata) are forced ou t of Eas t e rn Eu rope b y spruce forests of the Wes t Eu ropean t y p e (edif icator - - P. abies). The la rch forests of Larix karatschatica in the F a r E a s t a re forced out b y the Eas t Siber ian la rch forests of L. gmelinii. In t rogress ive hyb r id i z a t i on on which proceeded at the end of the T e r t i a r y be tween Picea and Tsuga species, and also be tween Larix and Pseudotsuga species, led to the c rea t ion of sect ion Ornorika spruces and sect ion Multiseriales larches. However , i t d id not c rea te evo lu t iona ry lines; the Picea and Larix species of these sect ions obviously became ext inct . The exper iments in crossing Larix sibirfca a n d Pseudotsuga taxi/ella car r ied out in 1972 and 1974 p roved the poss ib i l i ty of h y b r i d genesis of larches of Multiseriales section. The introgressive hybr id i za t ion in each known case, as wi th forest fo rming Conifers - - Picea, Larfx, Pinus, d id not create s table forms and d id no t open e v o l u t i o n a r y possibil i t ies.

L I T E R A T U R E C I T E D

AIeI)~RSON E. (1949): Introgressive Hybridization. -- New York. A~DERSO~ E. (1953): Introgressive hybridization. -- Biol. Rev., Cambridge, 28[3: 280--307. AI~DEnSOI~ E. et STEB~n~s G. L. Jr. (1954): Hybridization as an evolutionary stimulus. --Evolution,

Lancaster, 8/4: 378--388. BOBROV E. G. (1936): Gen. Carpinus. -- FI. U.R.S.S., Leningrad, 5: 254--262. BOBROV E. G. (1944): Ob osobennosti fiery erraticheskol oblasti. -- Soviet. Bet., Leningrad, 2:

3--20. BOBROV E. G. (1961): Introgressive Hybridization in the Flora of the Baikal part of Siberia. --

Dot. Journ., Leningrad, 46/3: 313--327. BOBROV E. G. (1971): Generic Picea historica et systematica. -- l~ovitates System., Leningrad,

7 (1970): 5--40. BOBROV E. G. (1972a): Die introgressive Hybridization in der Gattung Picea A. DIETR. -- Evo-

lution in Plants. -- In: Symposia Biol. Hung., Budapest, 12: 141--148. BoBber E. G. (1972b): Generis Larix MILL. historia et systematica -- Leningrad. Bomcov E. G. (1975a): What is Pinus ]unebris Ko~I. -- Bet. J., Leningrad, 60[5: 699--701. BOBROV E. G. (1975b): Pinus sylvestris in the Caucasus, the history and systematies. -- Bet. J . ,

Leningrad, 60/10: 1421-- 1433. BoBl~OV E. G. (1978): Coniferae silvificantes Unions Sovietici. -- Leningrad. ESAU K. (1945): BOBROV E. G.: Ob osobennosti fiery erratieheskoi oblasti. -- Biol. Abstr. Balti-

more, 196: 1082. [abstr. n ~ 10026] GROSSET E. G. (1958): The geographical distribution of Comus sanguinea s. 1. and history of the

broad-leaved forests of the European part of the U.S.S.R. -- Bull. Soc. Nat. Mosc., Moskva, 63]4: 77--85.

96 FOLIA GEOBOTANICA ET PHYTOTAXONO1KICA, 17, 1982

KNTAZ~VA L. A. (1978): Larch distant hybridization in Moscow region. -- Scientific bases of Conl- ferous trees Selections. -- Moskva.

M_~ov N. T. (1967): The genus Pinus. -- New York. PoPov M. (1927): The geographic-morphological method of Systematics and hybridization

process in nature. -- Bull. Appl. Bot. and Plant-breeding, Leningrad 17/1: 221--290. .STEBBINS G. L. (1959): Role of hybirdizatfon i~ evolution. -- Proe. Amer. Phil. Soc. Lancaster ,

103/2: 231--251. WRIG:Wr J. W. (1955): Species crossability in spruce in relation to distribution and t a x o n o m y . -

Forest Sci. U.S.A., 1/4: 319--349.

Received 21 April 1980